A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes.

Gerd P Bienert,Markus J Tamás,Michael Thorsen,Thomas P Jahn,Henrik R Nilsson,Manuela D Schüssler,Annemarie Wagner

doi:10.1186/1741-7007-6-26

Abstract

BackgroundArsenic is a toxic and highly abundant metalloid that endangers human health through drinking water and the food chain. The most common forms of arsenic in the environment are arsenate (As(V)) and arsenite (As(III)). As(V) is a non-functional phosphate analog that enters the food chain via plant phosphate transporters. Inside cells, As(V) becomes reduced to As(III) for subsequent extrusion or compartmentation. Although much is known about As(III) transport and handling in microbes and mammals, the transport systems for As(III) have not yet been characterized in plants.ResultsHere we show that the Nodulin26-like Intrinsic Proteins (NIPs) AtNIP5;1 and AtNIP6;1 from Arabidopsis thaliana, OsNIP2;1 and OsNIP3;2 from Oryza sativa, and LjNIP5;1 and LjNIP6;1 from Lotus japonicus are bi-directional As(III) channels. Expression of these NIPs sensitized yeast cells to As(III) and antimonite (Sb(III)), and direct transport assays confirmed their ability to facilitate As(III) transport across cell membranes. On medium containing As(V), expression of the same NIPs improved yeast growth, probably due to increased As(III) efflux. Our data furthermore provide evidence that NIPs can discriminate between highly similar substrates and that they may have differential preferences in the direction of transport. A subgroup of As(III) permeable channels that group together in a phylogenetic tree required N-terminal truncation for functional expression in yeast.ConclusionThis is the first molecular identification of plant As(III) transport systems and we propose that metalloid transport through NIPs is a conserved and ancient feature. Our observations are potentially of great importance for improved remediation and tolerance of plants, and may provide a key to the development of low arsenic crops for food production.

Highlights

Arsenic is a toxic and highly abundant metalloid that endangers human health through drinking water and the food chain
In Expression of specific Nodulin26-like Intrinsic Proteins (NIPs) from Arabidopsis sensitizes yeast Δfps1 to As(III) and Sb(III) To test whether plant aquaporin homologs transport As(III) and Sb(III), AtNIP1;1, AtNIP2;1, AtNIP5;1, AtNIP6;1 and AtNIP7;1 were heterologously expressed in the aquaglyceroporin deficient Δfps1 yeast mutant
Growth of yeast expressing Rat AQP9 (rAQP9) was reduced on medium containing 2 mM As(III) and completely repressed in the presence of 6 mM As(III), whereas the control yeast transformed with the empty vector grew well at concentrations up to 9 mM As(III)

Summary

Introduction

Arsenic is a toxic and highly abundant metalloid that endangers human health through drinking water and the food chain. Contaminated drinking water is the main source of arsenic intake in several parts of the world. The second largest source of arsenic for humans is through ingestion of food that has accumulated arsenic due to the irrigation of crop plants with polluted water [3]. In Argentina, arsenic concentrations of 300–400 parts per billion (ppb) were measured in soup and maize porridge [4] in villages where the drinking water was about 200 ppb [4,5], a concentration that is already considerably higher than the upper limit for drinking water of 10 ppb as recommended by the World Health Organization [2]. A detailed understanding of arsenic uptake and detoxification in plants is of great interest and is important for strategies in plant biotechnology for designing safer crops as well as for generating plants for the use in phytoremediation [7]

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